Organisms have evolved diverse reproductive strategies that impact the probability that their offspring survive to adulthood. Using morphological measurements in embryos and fry, gene expression analysis and hybrid crosses, we describe divergence in reproductive strategy between two closely related species of swordtail fish (Xiphophorus), which have internal fertilization and give birth to free-swimming fry. We find that one species, Xiphophorus malinche, has evolved larger offspring than its closest relative Xiphophorus birchmanni and dwarfs the offspring size of other species in the genus. The fry of X. malinche are more resilient to starvation than X. birchmanni, hinting that the evolution of large offspring size could be an adaptation to the challenging environments in which X. malinche are born. We also find evidence that X. malinche mothers provision nutrients to their offspring during embryonic development, the first time this process has been documented in the Xiphophorus genus. Moreover, in the ovary, we observe differential regulation of genes associated with maternal nutrient provisioning in other groups that use this reproductive strategy. Finally, we generated hybrid crosses between X. malinche and X. birchmanni to explore the impact of genetics and maternal environment on offspring size, finding that offspring size is at least in part genetically determined. Intriguingly, we find a low rate of survival in one cross direction and investigate the links between reproductive strategy and this asymmetric hybrid incompatibility.

Abstract Natural populations are often nonlinear and exhibit substantial variability. A central question is how stochasticity interacts with density-dependent regulation to shape population stability. We address this using four long-term time series of Trinidadian guppies and find that their dynamics are well described by a stochastic logistic model with multiplicative environmental noise. The model predicts that stochasticity does not merely add fluctuations around deterministic carrying capacity, but alters the equilibrium structure. Using stochastic bifurcation theory, we show that increasing noise shifts the most-probable population size below the deterministic equilibrium and can push populations closer to a noise-induced bifurcation, even when mean growth rates remain positive. The effects of stochasticity across populations align with known ecological differences among streams, particularly the effects of light level and seasonality. The analysis also identifies populations most sensitive to perturbations, which are not detected by standard early warning indicators. Temporal and spectral analyses further show that intrinsic growth rate governs local recovery, while seasonal variation interacts with density-dependence to shape longer-term population fluctuations. Together, our results show that stochasticity can alter resilience and vulnerability by reshaping ecological stability landscapes.

A recent study suggests that plants evolve reproductive isolation more rapidly than animals. Here, we present an alternative hypothesis: rather than revealing a difference between plants and animals, the study's results reveal how sexual conflict can shape the rate of evolution of reproductive isolation.

Placentas evolved nine times in the fish family Poeciliidae. Each time, the egg follicle is the maternal contribution to the placenta. In non-placental species, the follicle fully provisions the egg before fertilization. In placental species, provisioning continues throughout development, and the follicle becomes a more elaborate, well-vascularized organ. We generated transcriptomes for follicles from yolking eggs and developing embryos from two pairs of closely related placental and non-placental species that represent independent origins of placentation plus one non-placental outgroup. We identified genes expressed in eggs but not embryos of non-placental species that continue to be expressed during embryonic development in placental species. Their functions include the maternal transfer of nutrients and immunity. We then reconstructed the ancestral state of the non-placental common ancestor of each species pair and identified genes that were either upregulated or downregulated in developing embryos of placental species relative to non-placental species. These include clusters associated with lipid metabolism, immune response and tissue structure. The two placental lineages were convergent in the function of these genes, but few genes were in common between them. Thus, diverse gene regulatory changes converge on shared essential functions in the independent origins of a complex trait.

The evolution of placentation is predicted to intensify intergenomic conflicts between mothers and offspring over optimal levels of maternal investment by providing offspring opportunities to manipulate mothers into allocating more resources. Parent-offspring conflicts can result in the evolution of reproductive isolation among populations when conflicts resolve in different ways. Postzygotic reproductive isolation is hypothesized to evolve more rapidly following the evolution of placentation due to the predicted increase in conflict. We tested this hypothesis by performing interpopulation crosses within placental and nonplacental species of Poeciliopsis to determine if the relationship between genetic distance and measures of postzygotic reproductive success differed as function of reproductive mode. We did not observe any differences in offspring viability or sterility among crosses. Offspring size declined rapidly as a function of interpopulation genetic distance within the placental species, but not among our nonplacental species. The decrease in offspring size in the placental species was beyond normal variation, likely representing a major fitness cost, consistent with the prediction that negative epistatic interactions are evolving more quickly among populations in our placental species than the nonplacental species. We discuss how our results support the role parent-offspring conflicts play in the evolution of reproductive isolation and reproductive mode.

Several metrics have been proposed to measure phenotypic parallel evolution. All of these metrics stem from a geometric definition of parallel evolution in which two evolutionary trajectories are, literally, parallel or nonparallel to each other. Two metrics fit this definition: the interaction term between population and habitat in a two-factor ANOVA and a measure of the angle between two multivariate trajectories of evolution. A third metric is derived from the general direction of multivariate trajectories; although this might fit our intuition about parallel evolution, it does not fit the geometric definition. A fourth metric is based on the amount of variation explained by the habitat variable in a one-factor ANOVA (i.e., the R2). We show here that the R2 metric does not reliably measure any aspect of parallelism and should be avoided. We also discuss the importance of establishing proper ancestor-descendent relationships in attempting to use any of the valid metrics to quantify parallel evolution. Finally, because different metrics measure different aspects of evolutionary trajectories, we recommend being explicit about what one is trying to measure (angle, direction, or length of trajectories).

Diverse clades of fishes adapted to feeding on the benthos repeatedly converge on steep craniofacial profiles and shorter, wider heads. But in an incipient radiation, to what extent is this morphological evolution measurable and can we distinguish the relative genetic vs. plastic effects? We use the Trinidadian guppy (Poecilia reticulata) to test the repeatability of adaptation and the alignment of genetic and environmental effects shaping poecilid craniofacial morphology. We compare wild-caught and common garden lab-reared fish to quantify the genetic and plastic components of craniofacial morphology across 4 populations from 2 river drainage systems (n = 56 total). We first use micro-computed tomography to capture 3D morphology, then place both landmarks and semilandmarks to perform size-corrected 3D morphometrics and quantify shape space. We find a measurable, significant, and repeatable divergence in craniofacial shape between high-predation invertivore and low-predation detritivore populations. As predicted from previous examples of piscine adaptive trophic divergence, we find increases in head slope and craniofacial compression among the benthic detritivore foragers. Furthermore, the effects of environmental plasticity among benthic detritivores produce exaggerated craniofacial morphological change along a parallel axis to genetic morphological adaptation from invertivore ancestors. Overall, many of the major patterns of benthic-limnetic craniofacial evolution appear convergent among disparate groups of teleost fishes.

In this paper we draw on the wealth of biological and geological knowledge derived from over a century of work on the rich fauna and complex geology of Trinidad and Tobago, and the surrounding region, through petroleum exploration, academic research, and other studies. We use molecular studies from the last 20 years that address biogeography, phylogeography, phylogenetics, population genetics, morphology, and biogeography to link biological events to the geology, neotectonics, and geomorphology of this area of the southeast Caribbean and northern South America. We focus on studies that provide molecular timings of speciation, vicariance, and dispersal events to compare these to geological data. We first develop and review two relatively clear-cut biology-geology connections; we then review and speculate on other possible yet-unknown connections.

The viviparity-driven conflict hypothesis postulates that the evolution of matrotrophy (postfertilization maternal provisioning) will result in a shift from a pre- to postcopulatory mate choice and thus accelerate the evolution of postcopulatory reproductive isolation. Here, we perform artificial insemination experiments on Heterandria formosa, a matrotrophic poeciliid fish, to probe for evidence of postcopulatory female choice. We established laboratory populations from Wacissa River (WR) and Lake Jackson (LJ). The WR females normally produce larger offspring than the LJ females. We artificially inseminated females with sperm from each population or from both populations simultaneously. When LJ females were inseminated with sperm from WR and LJ males, they allocated fewer resources to WR-sired offspring than when they were inseminated with WR sperm alone. The LJ females carrying developing offspring sired by males from different populations were thus able to discriminate against non-resident males when allocating resources to developing young. The WR females, which normally produce larger offspring than LJ females, did not discriminate among males from different localities. These findings provide insights into the ability of females from one population to exercise a form of postcopulatory mate selection.

Coloration facilitates evolutionary investigations in nature because the interaction between genotype, phenotype and environment is relatively accessible. In a landmark set of studies, Endler addressed this complexity by demonstrating that the evolution of male Trinidadian guppy coloration is shaped by the local balance between selection for mate attractiveness versus crypsis. This became a textbook paradigm for how antagonistic selective pressures may determine evolutionary trajectories in nature. However, recent studies have challenged the generality of this paradigm. Here, we respond to these challenges by reviewing five important yet underappreciated factors that contribute to colour pattern evolution: (i) among-population variation in female preference and correlated variation in male coloration, (ii) differences in how predators versus conspecifics view males, (iii) biased assessment of pigmentary versus structural coloration, (iv) the importance of accounting for multi-species predator communities, and (v) the importance of considering the multivariate genetic architecture and multivariate context of selection and how sexual selection encourages polymorphic divergence. We elaborate these issues using two challenging papers. Our purpose is not to criticize but to point out the potential pitfalls in colour research and to emphasize the depth of consideration necessary for testing evolutionary hypotheses using complex multi-trait phenotypes such as guppy colour patterns.

Density-dependent selection, which promotes contrasting patterns of trait means at different population densities, has a long history in population genetics and ecology. The unifying principle from theory is that density-dependent selection operates on phenotypic traits whose values counter the effects of whatever ecological agent is limiting population growth, be it resource competition, predators, or pathogens. However, the complexity inherent in density dependence means that the same selective process can generate multiple outcomes, depending upon the details of how population density affects vital rates and the age or size structure of a population. Failure to appreciate the potential for multiple outcomes confounded many early studies of the process. Nonetheless, careful empirical work in laboratory studies, long-term field studies, and studies of sexual selection demonstrates the wide reach of density-dependent selection. The inconsistent outcomes observed in these studies call for renewed research into how the details of density dependence channel adaptive responses.

The blackstripe livebearer Poeciliopsis prolifica is a live-bearing fish belonging to the family Poeciliidae with high level of postfertilization maternal investment (matrotrophy). This viviparous matrotrophic species has evolved a structure similarly to the mammalian placenta. Placentas have independently evolved multiple times in Poeciliidae from nonplacental ancestors, which provide an opportunity to study the placental evolution. However, there is a lack of high-quality reference genomes for the placental species in Poeciliidae. In this study, we present a 674 Mb assembly of P. prolifica in 504 contigs with excellent continuity (contig N50 7.7 Mb) and completeness (97.2% Benchmarking Universal Single-Copy Orthologs [BUSCO] completeness score, including 92.6% single-copy and 4.6% duplicated BUSCO score). A total of 27,227 protein-coding genes were annotated from the merged datasets based on bioinformatic prediction, RNA sequencing and homology evidence. Phylogenomic analyses revealed that P. prolifica diverged from the guppy (Poecilia reticulata) ∼19 Ma. Our research provides the necessary resources and the genomic toolkit for investigating the genetic underpinning of placentation.

A major question in ecology is how often competing species evolve to reduce competitive interactions and facilitate coexistence. One untested route for a reduction in competitive interactions is through ontogenetic changes in the trophic niche of one or more of the interacting species. In such cases, theory predicts that two species can coexist if the weaker competitor changes its resource niche to a greater degree with increased body size than the superior competitor. We tested this prediction using stable isotopes that yield information about the trophic position (δ15 N) and carbon source (δ13 C) of two coexisting fish species: Trinidadian guppies Poecilia reticulata and killifish Rivulus hartii. We examined fish from locations representing three natural community types: (1) where killifish and guppies live with predators, (2) where killifish and guppies live without predators and (3) where killifish are the only fish species. We also examined killifish from communities in which we had introduced guppies, providing a temporal sequence of the community changes following the transition from a killifish only to a killifish-guppy community. We found that killifish, which are the weaker competitor, had a much larger ontogenetic niche shift in trophic position than guppies in the community where competition is most intense (killifish-guppy only). This result is consistent with theory for size-structured populations, which predicts that these results should lead to stable coexistence of the two species. Comparisons with other communities containing guppies, killifish and predators and ones where killifish live by themselves revealed that these results are caused primarily by a loss of ontogenetic niche changes in guppies, even though they are the stronger competitor. Comparisons of these natural communities with communities in which guppies were translocated into sites containing only killifish showed that the experimental communities were intermediate between the natural killifish-guppy community and the killifish-guppy-predator community, suggesting contemporary evolution in these ontogenetic trophic differences. These results provide comparative evidence for ontogenetic niche shifts in contributing to species coexistence and comparative and experimental evidence for evolutionary or plastic changes in ontogenetic niche shifts following the formation of new communities.

When females prefer mates with rare phenotypes, sexual selection can maintain rather than deplete genetic variation. However, there is no consensus on why this widespread and frequently observed preference might evolve and persist. We examine the fitness consequences of female preference for rare male color patterns in a natural population of Trinidadian guppies, using a pedigree that spans 10 generations. We demonstrate (i) a rare male reproductive advantage, (ii) that females that mate with rare males gain an indirect fitness advantage through the mating success of their sons, and (iii) the fitness benefit that females accrue through their “sexy sons” evaporates for their grandsons as their phenotype becomes common. Counter to prevailing theory, we show that female preference can be maintained through indirect selection.

Classic theory for density-dependent selection for delayed maturation requires that a population be regulated through some combination of adult fecundity and/or juvenile survival. We tested whether those demographic conditions were met in four experimental populations of Trinidadian guppies in which delayed maturation of males evolved when the densities of those populations became high. We used monthly mark-recapture data to examine population dynamics and demography in these populations. Three of the four populations displayed clear evidence of regulation. In all four populations, monthly adult survival rates were independent of biomass density or actually increased with increased biomass density. Juvenile recruitment, which is a combination of adult fecundity and juvenile survival, decreased as biomass density increased in all four populations. Demography showed marked seasonality, with greater survival and higher recruitment in the dry season than the wet season. Population regulation via juvenile recruitment supports the hypothesis that density-dependent selection was responsible for the evolution of delayed maturity in males. This body of work represents one of the few complete tests of density-dependent selection theory.

An outstanding question in biology is to what extent convergent evolution produces similar, but not necessarily identical, complex phenotypic solutions. The placenta is a complex organ that repeatedly evolved in the livebearing fish family Poeciliidae. Here, we apply comparative approaches to test whether evolution has produced similar or different placental phenotypes in the Poeciliidae and to what extent these phenotypes correlate with convergence at the molecular level. We show the existence of two placental phenotypes characterized by distinctly different anatomical adaptations (divergent evolution). Furthermore, each placental phenotype independently evolved multiple times across the family, providing evidence for repeated convergence. Moreover, our comparative genomic analysis revealed that the genomes of species with different placentas are evolving at a different pace. Last, we show that the two placental phenotypes correlate with two previously described contrasting life-history optima. Our results argue for high evolvability (both divergent and convergent) of the placenta within a group of closely related species in a single family.

The genetic basis of traits shapes and constrains how adaptation proceeds in nature; rapid adaptation can proceed using stores of polygenic standing genetic variation or hard selective sweeps, and increasing polygenicity fuels genetic redundancy, reducing gene re-use (genetic convergence). Guppy life history traits evolve rapidly and convergently among natural high- and low-predation environments in northern Trinidad. This system has been studied extensively at the phenotypic level, but little is known about the underlying genetic architecture. Here, we use four independent F2 QTL crosses to examine the genetic basis of seven (five female, two male) guppy life history phenotypes and discuss how these genetic architectures may facilitate or constrain rapid adaptation and convergence. We use RAD-sequencing data (16,539 SNPs) from 370 male and 267 female F2 individuals. We perform linkage mapping, estimates of genome-wide and per-chromosome heritability (multi-locus associations), and QTL mapping (single-locus associations). Our results are consistent with architectures of many loci of small-effect for male age and size at maturity and female interbrood period. Male trait associations are clustered on specific chromosomes, but female interbrood period exhibits a weak genome-wide signal suggesting a potentially highly polygenic component. Offspring weight and female size at maturity are also associated with a single significant QTL each. These results suggest rapid, repeatable phenotypic evolution of guppies may be facilitated by polygenic trait architectures, but subsequent genetic redundancy may limit gene re-use across populations, in agreement with an absence of strong signatures of genetic convergence from recent analyses of wild guppies.